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Performances of six eupelmid egg parasitoids from China on Japanese giant silkworm Caligula japonica with different host age regimes

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Abstract

The Japanese giant silkworm Caligula japonica Moore is an emerging defoliator pest of forest and fruit trees, causing severe economic losses in East Asia. To identify biological control agents for this pest, we comparatively evaluated six indigenous eupelmid egg parasitoids (Anastatus fulloi, A. gansuensis, A. japonicus, A. meilingensis, Mesocomys albitarsis and M. trabalae) from China, in terms of their performances (number of parasitized eggs, developmental time, offspring emergence and sex ratio) on C. japonica eggs of four different ages (0, 10, 20 and 30-d old). Results showed that all six parasitoids readily parasitized C. japonica eggs of all tested ages, but A. japonicus was the most efficient species based on the number of parasitized eggs, followed by M. albitarsis and M. trabalae, and the other three parasitoid species. All four Anastatus species parasitized more old than young eggs, while M. albitarsis did not show a strong host age preference and M. trabalae parasitized the oldest less than young eggs. For all host ages, developmental time was longest in A. gansuensis and shortest in M. albitarsis, offspring emergence was high (> 90%), and progeny was strongly female biased (> 70%) among all parasitoids except for A. gansuensis which produced all female progeny. Portions of A. japonicus offspring (< 13.1%) entered diapause as pre-pupae. Accordingly, A. japonicus, M. albitarsis and M. trabalae were identified as the most suitable agents against C. japonica. This information may also help improve rearing and field-release protocols, in terms of host age-related effects on these parasitoids.

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References

  • Abarenkov K (2019) Life Sciences EUO, Estonian University of Life Sciences. PlutoF. Occurrence dataset. https://doi.org/10.15156/bio/587441 accessed via GBIF.org on 2019–12–28. https://www.gbif.org/occurrence/1148336835. Accessed 28 Dec 2019

  • Abram PK, Talamas EJ, Acheampong S, Mason PG, Gariepy TD (2019) First detection of the samurai wasp, Trissolcus japonicus (Ashmead) (Hymenoptera, Scelionidae), in Canada. J Hym Res 68:29–36

    Google Scholar 

  • Ai H, Zhao S, She Z (2000) A study on natural enemies of Euproctis pseudoconspersa Strand. Entomol J East China 9:67–72

    Google Scholar 

  • Boyadzhiev P, Mirchev P, Georgiev G (2017) Species of the Genus Ooencyrtus Ashmead, 1900 (Hymenoptera: Encyrtidae), egg parasitoids of Thaumetopoea solitaria (Lepidoptera: Notodontidae) in Bulgaria. Acta Zool Bulg 1:107–112

    Google Scholar 

  • Chen YM, Gibson GAP, Peng LF, Iqbal A, Zang LS (2019) Anastatus Motschulsky (Hymenoptera, Eupelmidae): egg parasitoids of Caligula japonica Moore (Lepidoptera, Saturniidae) in China. ZooKeys 881:109–134

    PubMed  PubMed Central  Google Scholar 

  • Chen YM, Sun JW, Iqbal A, Lu R, Wang H, Zang LS (2020) An investigation of Caligula japonica (Lepidoptera: Saturniidae) egg distribution and associated parasitoids on walnut trees (Juglans regia L.) in northwestern China. Int J Pest Manag. In press

  • Clausen CP (1927) The bionomics of Anastatus albitarsis Ashm., parasitic in the eggs of Dictyoploca japonica Moore (Hymen.). Ann Entomol Soc Am 20:461–473

    Google Scholar 

  • Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106

    CAS  PubMed  Google Scholar 

  • Dong DJ (2013) Toxicity determination and control effect of several pesticides against Dictyoploca japonica Butler. Forest Pest Dis 32:38–40

    Google Scholar 

  • Fang HL, Lian YY, Zhu JR, Zhang AX (1995) Study on the dynamics of Anastatus albitarsis in the forest. J Zhejiang For Coll 12:73–78

    Google Scholar 

  • Fischbein D, Corley JC (2015) Classical biological control of an invasive forest pest: a world perspective of the management of Sirex noctilio using the parasitoid Ibalia leucospoides (Hymenoptera: Ibaliidae). Bull Entomol Res 105:1–12

    CAS  PubMed  Google Scholar 

  • Fischbein D, Lantschner MV, Corley JC (2019) Modelling the distribution of forest pest natural enemies across invaded areas: towards understanding the influence of climate on parasitoid establishment success. Biol Control 132:177–188

    Google Scholar 

  • Gerling D, Erel E, Guershon M, Inbar M (2009) Bionomics of Encarsia scapeata Rivnay (Hymenoptera: Aphelinidae), tritrophic relationships and host-induced diapause. Biol Control 49:201–206

    Google Scholar 

  • Gibson GAP (1995) Parasitic wasps of the subfamily Eupelminae: classification and revision of world genera (Hymenoptera: Chalcidoidea: Eupelmidae). Mem Entomol Int 5:1–421

    Google Scholar 

  • Gibson GAP (1997) Chapter 2. Morphology and Terminology. In: Gibson GAP, Huber JT, Woolley JB (eds) Annotated keys to the genera of nearctic chalcidoidea (hymenoptera). NRC Research Press, Ottawa, pp 16–44

    Google Scholar 

  • Gibson GAP (2011) The species of Eupelmus (Eupelmus) Dalman and Eupelmus (Episolindelia) Girault (Hymenoptera: Eupelmidae) in North America north of Mexico. Zootaxa 2951:1–97

    Google Scholar 

  • Gibson GAP, Fusu L (2016) Revision of the Palaearctic species of Eupelmus (Eupelmus) Dalman (Hymenoptera: Chalcidoidea: Eupelmidae). Zootaxa 4081:1–331

    PubMed  Google Scholar 

  • Hassan SA, Liscsinszky H, Zhang G (2004) The oak-silkworm egg Antheraea pernyi (Lepidoptera: Anthelidae) as a mass rearing host for parasitoids of the genus Trichogramma (Hymenoptera: Trichogrammatidae). Biocontrol Sci Techn 14:269–279

    Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, de Waard JR (2003) Biological identifications through DNA barcodes. P Roy Soc B-Biol Sci 270:313–321

    CAS  Google Scholar 

  • Heimpel GE, de Boer JG (2008) Sex determination in the hymenoptera. Annu Rev Entomol 53:209–230

    CAS  PubMed  Google Scholar 

  • Hirose Y (1964) The activity of the egg parasite of the pine-moth, Dendrolimus spectabilis Butler in the Japanese black pine forest on the sea coast. Sci Bull Fac Agr Kyushu Univ 21:13–24

    Google Scholar 

  • Hopper KR (1999) Risk-spreading and bet-hedging in insect population biology. Annu Rev Entomol 44:535–560

    CAS  PubMed  Google Scholar 

  • Hou YY, Yang X, Zang LS, Zhang C, Monticelli LS, Desneux N (2018) Effect of oriental armyworm Mythimna separata egg age on the parasitism and host suitability for five Trichogramma species. J Pest Sci 91:1181–1189

    Google Scholar 

  • Huang NX, Jaworski CC, Desneux N, Zhang F, Yang PY, Wang S (2020) Long-term, large-scale releases of Trichogramma promotes pesticide decrease in maize in Jilin province, Northern China. Entomol Gen. https://doi.org/10.1127/entomologia/2020/0994

    Book  Google Scholar 

  • Iqbal A, Chen YM, Hou YY, Zhang L, Desneux N, Zang LS (2019) Factitious host species impact on the outcome of multiparasitism between egg parasitoids. J Pest Sci 92:1261–1269

    Google Scholar 

  • Kawasaki H, Sato H (1985) The tanning agent in the silk of the Japanese giant silkmoth, Dictyoploca japonica Butler. Insect Biochem 15:681–684

    CAS  Google Scholar 

  • Li DS, Liao CY, Zhang BX, Song ZW (2014) Biological control of insect pests in litchi orchards in China. Biol Control 68:23–36

    Google Scholar 

  • Li TH, Tian CY, Zang LS, Hou YY, Ruan CC, Yang XB, Lucie M, Desneux N (2019) Multiparasitism with Trichogramma dendrolimi on egg of Chinese oak silkworm, Antheraea pernyi, enhances emergence of Trichogramma ostriniae. J Pest Sci 92:707–713

    Google Scholar 

  • Liu SY, Luo YF (2008) Application of Beauveria bassiana (Balsamo) Vuillemin for the control of Dictyoploca japonica Moore. Guizhou For Sci Techn 1:36–39

    Google Scholar 

  • Mills N (2010) Egg parasitoids in biological control and integrated pest management. In: Consoli FL, Parra JPR, Zucchi RA (eds) Egg parasitoids in agroecosystems with emphasis on Trichogramma. Springer, New York, pp 389–411

    Google Scholar 

  • Monti MM, Francesco N, Liberata G, Marco G, Umberto B (2016) No evidence of parthenogenesis-inducing bacteria involved in Thripoctenus javae thelytoky: an unusual finding in Chalcidoidea. Entomol Exp App 160:292–301

    CAS  Google Scholar 

  • Morris R, Fellowes M (2002) Learning and natal host influence host preference, handling time and sex allocation behaviour in a pupal parasitoid. Behav Ecol Sociobiol 51:386–393

    Google Scholar 

  • Narasimham AU, Sankaran T (1982) Biology of Anastatus umae (Hymenoptera: Eupelmidae), an oothecal parasite of Neostylopyga rhombifolia. Colemania 1:135–140

    Google Scholar 

  • Nashiki Y (2019) Insect specimens of Komatsu City Museum. Version 1.1. National Museum of Nature and Science, Japan. Occurrence dataset. https://doi.org/10.15468/8reiif accessed via https://www.gbif.org/ on 2019-12-28. Accessed 28 Dec 2019

  • Nugnes F, Gebiola M, Monti MM, Gualtieri L, Giorgini M, Wang J, Bernardo U, Munderloh UG (2015) Genetic diversity of the invasive gall wasp Leptocybe invasa (Hymenoptera: Eulophidae) and of its Rickettsia endosymbiont, and associated sex-ratio differences. PLoS ONE 10:e0124660

    PubMed  PubMed Central  Google Scholar 

  • Nurindah, Bronwen WC, Gordh G (1999) Influence of rearing hosts on host size acceptance by Trichogramma australicum. Biocontrol 44:129–141

    Google Scholar 

  • Ohno Y, Umeki K, Watanabe I, Takiya M, Terazawa K, Hara H, Matsuki S (2008) Variation in shoot mortality within crowns of severely defoliated Betula maximowicziana trees in Hokkaido, northern Japan. Ecol Res 23:355–362

    Google Scholar 

  • Pizzol J, Desneux N, Wajnberg E, Thiéry D (2012) Parasitoid and host egg ages have independent impact on various biological traits in a Trichogramma species. J Pest Sci 85:489–496

    Google Scholar 

  • Qiao X, Wang YC, Wu G, Wang SY, Hu JZ, Liu TX, Feng SQ (2014) Occurrence reasons and control measures of Caligula japonica in Longnan city of China. Plant Dis Pests 5:38–41

    Google Scholar 

  • Qu YY, Xiao D, Li JY, Chen Z, Biondi A, Desneux N, Gao XW, Song D (2015) Sublethal and hormesis effects of imidacloprid on the soybean aphid Aphis glycines. Ecotoxicology 24:479–487

    CAS  PubMed  Google Scholar 

  • Quicke DJ (1997) Parasitic Wasps. Chapman and Hall, London

    Google Scholar 

  • Rabeling C, Kronauer DJ (2013) Thelytokous parthenogenesis in eusocial hymenoptera. Annu Rev Entomol 58:273–292

    CAS  PubMed  Google Scholar 

  • SAS Institute (2010) SAS/STAT v.9.1. SAS Institute, Cary, NC, USA

  • Sheng JK, Wang GH, Yu YX, Yu JC (1997) Four new species of Anastatus Motschulsky (Hymenoptera: Euplemidae) from China. Entomotaxonomia 19:58–64

    Google Scholar 

  • Sheng JK, Yu YX (1998) Two new species of Anastatus Motschulsky from China (Hymenoptera, Chalcidoidea, Eupelmidae). Wuyi Sci J 14:5–8

    Google Scholar 

  • Simon JC, Delmotte F, Rispe C, Crease T (2003) Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals. Biol J Linn Soc 79:151–163

    Google Scholar 

  • Smith SM (1996) Biological control with Trichogramma: advances, success, and potential of their use. Annu Rev Entomol 41:375–406

    CAS  PubMed  Google Scholar 

  • Stahl JM, Babendreier D, Haye T (2018a) Using the egg parasitoid Anastatus bifasciatus against the invasive brown marmorated stink bug in Europe: can non-target effects be ruled out? J Pest Sci 91:1005–1017

    Google Scholar 

  • Stahl JM, Babendreier D, Haye T (2018b) Life history of Anastatus bifasciatus, a potential biological control agent of the brown marmorated stink bug in Europe. Biol Control 129:178–186

    Google Scholar 

  • Sullivan C, Griffiths K, Wallace D (1977) Low winter temperatures and the potential for establishment of the egg parasite Anastatus disparis (Hymenoptera: Eupelmidae) in Ontario populations of the gypsy moth. Can Entomol 109:215–220

    Google Scholar 

  • Talamas EJ, Herlihy MV, Dieckhoff C, Hoelmer KA, Buffington ML, Bon M-C, Weber DC (2015) Trissolcus japonicus (Ashmead) emerges in North America. J Hymenopt Res 43:119–128

    Google Scholar 

  • Teng XW, Ni LX (1989) Bionomics of Pseudanastatus albitarsis Ashmead and its utiuzation for control of Dendrolimus punctatus Walker. Acta Entomol Sin 32:451–458

    Google Scholar 

  • Tetsu A, Ikuo I, Fumihiko K, Chiharu S (1974) Electron microscope observations on the maturation process of the Nucleopolyhedrosis viruses of the oriental tussock moth, Euproctis subflava Bremer and the Japanese giant silkworm, Dictyoploca japonica Butler. Jap J App Entomol Z 18:189–197

    Google Scholar 

  • Vanden Berg MA (1971) Studies on the induction and termination of diapause in Mesocomys pulchriceps Cam. (Hymenoptera: Eupelmidae) an egg parasite of Saturniidae (Lepidoptera). Phytophylactica 3:85–88

    Google Scholar 

  • Vinson SB (1976) Host selection by insect parasitoids. Ann Rev Entomol 21:109–133

    Google Scholar 

  • Vinson SB (1998) The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biol Control 11:79–96

    Google Scholar 

  • Wang XG, Messing RH (2004) Fitness consequence of body size-dependent host species selection in a generalist ectoparasitoid. Behav Ecol Sociobiol 56:513–522

    Google Scholar 

  • Wang YX, Qiao X, Wang ZK (2012) Pharmacodynamic study on different insecticide for Caligula japonica Moore. Modern Agr Sci Techn 14:95–96

    Google Scholar 

  • Watt TJ, Duan JJ, Tallamy DW, Judith HG (2015) Effect of parasitoid: host ratio and group size on fitness of Spathius galinae (Hymenoptera: Braconidae): implications for mass-rearing. J Econ Entomol 108:951–956

    PubMed  Google Scholar 

  • Weisenburger DD (1993) Human health effects of agrichemical use. Hum Pathol 24:571–576

    CAS  PubMed  Google Scholar 

  • Yang BS, Li J, Li YR, Wang Z (2008a) Genetic diversity assessment of Dictyoploca japonica from different areas. Chin Bull Entomol 45:418–421

    CAS  Google Scholar 

  • Yang BS, Zhang XK, Cao LJ, Qin L (2008b) Biological characteristics of Dictyoploca japonica Moore and the technology for prevention and control. Agrochemicals 47:153–154

    CAS  Google Scholar 

  • Yang ZQ, Wei JR, Wang XY (2006) Mass rearing and augmentative releases of the native parasitoid Chouioia cunea for biological control of the introduced fall webworm Hyphantria cunea in China. Biocontrol 51:411–418

    Google Scholar 

  • Yao YX, Yang ZQ, Zhao WX (2009) Descriptions of four new species in the genus Mesocomys (Hymenoptera, Eupelmidae) parasitizing eggs of defoliators from China. Acta Zootaxonomica Sin 34:155–160

    Google Scholar 

  • Yuan XH, Song LW, Zhang JJ, Zang LS, Zhu L, Ruan CC, Sun GZ (2012) Performance of four Chinese Trichogramma species as biocontrol agents of the rice striped stem borer, Chilo suppressalis, under various temperature and humidity regimes. J Pest Sci 85:497–504

    Google Scholar 

  • Zang LS, Wang S, Zhang F, Desneux N (2021) Biological control with Trichogramma in China: history, present status and perspectives. Annu Rev Entomol. https://doi.org/10.1146/annurev-ento-060120-091620

    Article  PubMed  Google Scholar 

  • Zchori-Fein E, Gottlieb Y, Kelly SE, Brown JK, Wilson JM, Karr TL, Hunter MS (2001) A newly discovered bacterium associated with parthenogenesis and a change in host selection behavior in parasitoid wasps. P Natl Acad Sci USA 98:12555–12560

    CAS  Google Scholar 

  • Zchori-Fein E, Perlman SJ (2004) Distribution of the bacterial symbiont Cardinium in arthropods. Mol Ecol 13:2009–2016

    CAS  PubMed  Google Scholar 

  • Zhang JJ, Ren BZ, Yuan XH, Zang LS, Ruan CC, Sun GZ, Shao XW (2014) Effects of host-egg ages on host selection and suitability of four Chinese Trichogramma species, egg parasitoids of the rice striped stem borer, Chilo suppressalis. Biocontrol 59:159–166

    CAS  Google Scholar 

  • Zhao C, Xia Y, Guo Y, Li M, Zhang B, Li D (2019) The study on diapause induction in Anastatus japonicus Ashmead. Chin J Biol Control 35:282–287

    Google Scholar 

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Acknowledgments

We are grateful to Dr. Gary Gibson (Honorary Research Associate, Agriculture and Agri-Food Canada, Canadian National Collection of insects) for the identification of six Eupelmidae species. This research was funded by the National Key R&D Program of China (Nos: 2017YFE0104900 and 2017YFD0201000), and Gansu Provincial Fiscal Science and Technology Award and Compensation Project (2018-01).

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Authors and Affiliations

  1. Jilin Engineering Research Center of Resource Insects Industrialization, Institute of Biological Control, Jilin Agricultural University, Changchun, China

    Yong-Ming Chen, Xing-Ran Qu, Tian-Hao Li, Asim Iqbal & Lian-Sheng Zang

  2. United States Department of Agriculture, Agricultural Research Service, Beneficial Insects Introduction Research Unit, Newark, DE, 19713, USA

    Xingeng Wang

  3. Institute of Walnut, Longnan Economic Forest Research Institute, Wudu, China

    Zhi-Yong Ren

  4. Université Côte d’Azur, INRAE, CNRS, UMR ISA, 06000, Nice, France

    Nicolas Desneux

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  1. Yong-Ming Chen
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Chen, YM., Qu, XR., Li, TH. et al. Performances of six eupelmid egg parasitoids from China on Japanese giant silkworm Caligula japonica with different host age regimes. J Pest Sci 94, 309–319 (2021). https://doi.org/10.1007/s10340-020-01271-1

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